Prevalence and Associated Risk Factors of Intestinal Parasites among Children under Five Years of Age Attended at Bachuma Primary Hospital, West Omo Zone, Southwest Ethiopia: A Cross-Sectional Study

Background In regions of the world with low resources, such as Ethiopia, intestinal parasite diseases are still highly prevalent, especially in children. Poor personal and environmental hygiene, as well as unsafe and low-quality drinking water, are the main causes of this. This investigation aimed to determine the frequency of intestinal parasites and risk factors among children under 5 years age at Bachuma Primary Hospital in 2022. Materials and Methods : A cross-sectional study was carried out from October 2022 to December 2022 at Bachuma Primary Hospital, West Omo Zone, Southwest Ethiopia. Stool sample was collected from randomly selected children who were ordered to have their stool examined at the hospital laboratory and wet mount was prepared using normal saline to detect the different stage of intestinal parasites microscopically. Moreover, data related to the sociodemographic and associated risk factors was collected using a structured questionnaire. Descriptive statistics were computed to describe the characteristics of the study participants and determine the prevalence of intestinal parasites. Data were entered into Epi-data manager and analysed using statistical packages for social sciences (SPSS) version 25.0, respectively. Bivariate and multivariate logistic regression analyses were performed, with variables with a p value of <0.05 considered statistically significant. Result : Infection with at least one intestinal parasite among children was 29.4% (95% CI: 24.5–34.7). Ascaris lumbricoide and Giardia lamblia were responsible for 8% (26/323) and 4% (13/323) of the prevalence of helminth and protozoans, respectively. A multivariate logistic regression analysis revealed that children whose residence was rural had an adjusted odds ratio (AOR) of 5.048 (p=0.001), those who did not wash their hands before meals had an AOR of 7.749 (p=0.001), a child with not trimmed fingernails had an AOR of 2.752 (p=0.010), a child who frequently experienced stomach pain and whose source of water was pond had an AOR of 2.415 (p=0.028) and 3.796 (p=0.040), respectively. Conclusion In this study, the prevalence of intestinal parasites recorded was low. Rural residency, absence of child hand washing practice before meal, and not trimming fingernail were among factors significantly associated with intestinal parasite infection.


Introduction
1.1. Background. Infections with helminths and protozoa of intestinal parasites are very common worldwide, particularly in developing nations. According to estimates by the World Health Organization (WHO), 3.5 billion people are impacted and 200,000 deaths are reported annually [1]. Intestinal parasites are frequently transmitted by contaminated food or drinking water, but may also be spread from person to person through fecal-oral contact. Te prevalence of these parasitic infections varies in diferent parts of the world [1].
However, in developing nations, the issue is exacerbated by geographic, economic, and unpredictable factors such as natural disasters. Te socioeconomic and health of populations with limited resources are signifcantly afected by intestinal parasites, which are among the most widespread human parasites [2]. Due to many circumstances, the microgeographical distribution of these illnesses may greatly range from one location to another [3].
Today, parasitic infection is a more prevalent and widespread problem due to poor sanitary and afects all people according to conditions, shoe-wearing habits, lack of proper latrines, and other socioeconomic and geographic factors in most regions of the world. Studies conducted in diferent countries showed that there is a gap in the evaluation of the prevalence of intestinal parasites for children at the primary hospital level. Although intestinal parasite infection is a common public health problem all over the world, it is a more concerning issue in Ethiopia. Wet mount stool examination technique was used to identify parasite species and their prevalence in children under fve years at a local primary hospital since wet mount stool examination is the method of choice across health facilities in the country because of its simplicity and afordability.
Tis study was conducted in West Omo zone, Southwest Ethiopia which is one of the remote/far to reach areas of the country with low coverage of infrastructure and with scanty health facilities where information related to the prevalence of intestinal parasites among vulnerable groups such as children under fve year was not sufciently addressed. So, this study could bring important information on the prevalence of intestinal parasites in these risky population and serve as baseline data for an efective intervention in the study area.

Study Design.
A health facility-based cross-sectional study was employed among children under fve years who came to Bachuma primary hospital seeking medical services.

Study Area and Period.
Te study was conducted at Bachuma Primary Hospital from October to December 2022. Te study site is found in Bachuma town, which has one public and four private health facilities. Te town is in the West Omo Zone, southwest part of Ethiopia, 565 km away from Addis Ababa, the capital city of Ethiopia. Bachuma has high land climate conditions, heavy rainfall, warm temperatures, and a long-wet period. Based on the 2010 census conducted by the CSA, the total population of the town is 3894, of whom 881 are men and 2013 are women. But the hospital health service deliveries covered a larger population and diferent catchment areas (an estimated population of more than 300,000 from hospital information).

Source Population.
Children under fve years of age attended at Bachuma Primary Hospital from October to December 2022.

Study Population.
Children under fve years of age who seek laboratory investigations for intestinal parasites during the study period.

Inclusion and Exclusion
Criteria. Children under fve years of age who experienced diarrhea during their visit of the hospital laboratory and those without diarrhea but with other related symptoms sent to the laboratory with prescriptions of stool examination during the study period were included whereas, those who had taken antiparasitic drugs in one month period before examination and whose parents/ guardians refuse to give sociodemographic and other related data were excluded.
2.6. Sample Size and Sampling Technique 2.6.1. Sample Size. Te sample size was calculated by using the following formula: where n is the minimum sample size required, z is the critical value for a given confdence interval, and p is the expected intestinal prevalence at Bachuma Primary Hospital.
where n represents minimum sample size, p represents prevalence rate (26.6%) [4] taken from a study conducted on intestinal parasites among children under fve years at public health facilities in Hawassa, (Zα/2) represents standards normal variable (1.96), and d represents margin of sampling error (5%). Adding a 10% nonresponse rate, the fnal sample size was (n) 300 + 30.0 � 330.

Sampling Technique.
A systematic random sampling technique was employed to select the children to participate in the study from those sent to the laboratory department of the hospital for stool examination. Te sampling frame was obtained from the registered information by the diferent health facilities in the catchment of the area where this study was conducted and accordingly there were about 1286 children under the age of fve years who got services such as immunization/ vaccination at diferent health facilities in the catchment. Te K th interval calculated from the population and the sample size was (3.89 ≈ 4). Hence, the study participants (only children under fve years) who met the inclusion criteria were picked every fourth after randomly selecting the frst child by lottery system until the desired sample size was reached. Finally, 323 children who fulfl the inclusion criteria were included in the study.

Data Collection and Analysis
3.1. Data Collection. One gram (1 gm) of stool sample was collected from each child whose parents or guardians signed an informed written consent form and expressed a desire to participate in the study. A pretested structured questionnaire was used to collect data related to sociodemographic characteristics and other independent variables. Te data generated from the laboratory results and questionnaires were summarized for the fnal analysis.

Stool Wet Mount
Technique. Wet mount stool sample examination is the most used method of intestinal parasite detection in almost all the health facilities in Ethiopia. Tis method is simple and easy to perform with little fnancial investment compared to other techniques such as concentration technique and molecular level tests but with low sensitivity. Te wet mount slide was prepared taking 2 milligrams of either diarrheic or nondiarrheic stool sample from the children and the slides were examined microscopically under both 10x and 40x objectives of light microscope by two laboratory technicians to identify the diferent stages of protozoans and helminths. To prepare the wet mount, a microscope slide, cover slip, and a drop or two drop of normal saline were used. Tickness of the wet mount was made to the standard to enable detection of all the possible stages of intestinal parasites.

Data Analysis.
Epi data was used to enter data and analysed using SPSS version 25. Descriptive statistics were used to show the prevalence of intestinal parasites. Tables and fgures were used to present the data. Binary logistic analysis was performed frst, and variables with a p value <0.25 were considered candidates for multivariable logistic regression for the fnal analysis. An adjusted odds ratio (AOR) with a 95% confdence interval (CI) was reported. In the multivariable logistic regression analysis, variables with a p value of less than 0.05 were signifcantly associated with intestinal parasites infection.

Data Quality Control.
Te standard operating procedure (SOP) was strictly followed for the stool sample examination process. To avoid a technical error that encountered the quality of normal saline was checked during sample collection and microscopic examination, that is, internal quality control was conducted. Te data collection format of each data was checked daily for completeness of missed or other relevant data during data collection, as well as by the principal investigators. Special emphasis was given to diarrhea stool samples. Te consistency and completeness were checked by the investigators and the questionnaire was pretested at the Mizan-Tepi Teaching Hospital.
To ensure the quality of the investigation, two laboratory technicians examine the slides independently and their readings were compared. Discordant results were immediately resolved with a discussion among them and in consultation with an experienced laboratory expert.

Sociodemographic Characteristics.
A total of 323 children with an age range of 6 months to 59 months and each child's parents or caregivers participated in this study. More than half of the children were female, representing a higher proportion of intestinal parasite infections than their male counterparts. Intestinal parasite infection was relatively higher in the age category of 12-36 months compared to those under 1 year and over 3 years. Out of 323 parents/ guardians who participated in this study, 43.7% of them earn 500-1000 Ethiopian Birrs monthly. Of the total study participants, 28.2% were illiterate and among daily laborers, a relatively high number of parents/caregivers participated in the study (Table 1).
In this study, two-thirds of the houses were found to be uncemented, and more than two-thirds of caregivers/ mothers did not wash their hands with soap and clean water before feeding their child, but more than half of them did so after using the toilet. More than one-third of the children in this study use water from a stream, and more than half of them have trimmed fngernails. More than three-fourths of the children ate vegetables and fruits that were not washed ( Table 2).

Intestinal Parasite Infections-Related Factors.
All variables with a p value of <0.25 were taken to the multivariate logistic regression model accordingly. Some of the associated factors showed a signifcant association with the infection of intestinal parasites in a child: children whose residence was in rural AOR (5.048; 95% CI: 2.166-11.764) were more likely to be infected with intestinal parasites than those from urban, those who did not wash their hands before meal AOR (7.749; 95% CI: 2.684-22.373) were 7.749 times more likely to contract intestinal parasite infection compared to their counterparts. Moreover, children whose fngernails were not trimmed and who experienced stomach pain frequently were more than twofold more susceptible to intestinal parasitic infection with AOR (2.752; 95% CI: 1.280-5.917) and (2.415; 95% CI: 1.100-5.302), respectively. Te source of drinking water appeared to play a signifcant role in increasing the risk of intestinal parasite infection, with those who used water from a pond have AOR of (3.796; 95% CI: 1.060-13.591) ( Table 3).

Prevalence of Intestinal Parasites in Relation to Certain
Clinical Symptoms. More than one-third of the study participants/children experienced abdominal pain before stool sample collection, and more than one-fourth of the children also had diarrhea during the study period. Tose with gastrointestinal tract urgency accounted for 16% of the participants (Figure 2).

Discussion
Successful preventive and therapeutic interventions towards intestinal parasitic infections emanates from understanding of the distribution and extent of intestinal parasitic infection in a given community. Tis study assessed the prevalence as well as the associated factors of intestinal parasite infection.  [21], and South Ethiopian Hospital (21.2%) [22]. Te reason for these variations may be attributed more to the diference in geographical locations of the study areas, that is, the current study was conducted in relatively less urbanized parts of the country with low coverage infrastructures such as health facilities. Tis study revealed that children from rural areas were more likely to have intestinal parasite infections than children from urban areas, and those who did not wash their hands before meals were 7.749 times more likely to contract an intestinal parasite infection compared to their counterparts. Tis might be due to the low coverage of deworming services in rural areas compared to urban dwellers. Moreover, children whose fngernails were not trimmed and who experienced stomach pain frequently were more than twice as susceptible to Journal of Tropical Medicine intestinal parasitic infection. Tose children whose fngernails were not shortened or trimmed were 2.752 times prone to intestinal parasite infection contributing 18% of the prevalence, which is supported by similar studies conducted in Ethiopia [23]. Tis could be attributed to the lack removal of accumulated dirt containing parasite eggs in fngernails which could serve as source infection [24]. Te source of drinking water also appeared to play a great role in increasing the chance of getting an intestinal parasite infection, hence children who used water from pond accounted for a relatively high number of the positive cases. Tis might be due to contamination of water and food with human waste during open feld defecation. In addition, lack of awareness about the importance of hand washing practices after defecation can lead to easy contamination of people through food. According to a study from Côte d'Ivoire; poor sanitation and hygiene practices are linked to intestinal protozoa and helminth infections that are transferred through the soil [25]. Te distribution and prevalence of various species of intestinal parasites difer from region to region because of several environmental, social, and geographical and other factors. In this study, the wet mount microscopy method was used to determine the prevalence of intestinal parasites although molecular assays and concentration techniques could best estimate the burden of intestinal parasites.

Limitation of the Study. Molecular tests and other
concentration techniques could best estimate the prevalence of intestinal parasites compared to the conventional microscopy method which has low sensitivity. Furthermore, diferentiation between the morphologically identical species of Entamoeba was not within the scope of this study, as only wet mount microscopy was used.

Conclusion and Recommendation
A low prevalence of intestinal parasite infection was recorded among the children under fve years of age who participated in this study. Ascaris lumbricoide, Trichuris trichiura, and Giardia lamblia were the most common parasites found in the study. Rural residency, not washing hands before meal, not trimming fngernails, and using unclean water (from streams and ponds) were some of the factors signifcantly associated with intestinal parasitic infection. Diagnostic techniques with better detection ability such as formol-ether concentration technique and molecular based tests could ofer better result than what is found by wet mount in this study.

IP:
Intestinal parasite IPIS: Intestinal parasitic infections NGO: Non-Governmental Organization WHO: World Health Organization BPH: Bachuma primary hospital SOP: Standard operating procedure LPF: Low-power feld HPF: High-power feld KAP: Knowledge, attitude, and practice.

Data Availability
Te data related to this study are available from the corresponding author upon reasonable request.

Ethical Approval
Ethical approval was obtained from the institutional review board of the college of medicine and health science at Mizan-Tepi University with approval number CHS/000984/ 22. Te Bachuma primary Hospital administrative body gave a legal permission letter for the study to proceed. Te objective of the study was verbally explained to the laboratory personnel and the administrative body of the hospital. Written informed consent was obtained from the parents/ guardians of the study participants before data collection.

Conflicts of Interest
Te authors declare that they have no conficts of interest. sociodemographic characteristics of the children such as age, sex, and resident; sociodemographic characteristics of the parents/guardians (age, sex, resident, educational status, occupational status, and family monthly income); and questions related to associated risk factors of intestinal parasitic infection and clinical manifestation of children under the age of fve. (Supplementary Materials)